Dis Tri Bu Tion of Cla Do Cera Com Mu Ni Ties Across a Climate Gradi Ent in Shallow Lakes from Croatia to Hungary: a Prelimi Nary Study

Studia Quaternaria, vol. 29 (2012): 45–52.

DIS TRI BU TION OF CLA DO CERA COM MU NI TIES ACROSS A CLIMATE GRADI ENT IN SHALLOW LAKES FROM CROATIA TO HUNGARY: A PRELIMI NARY STUDY

Csilla Kövér1, János Korponai 1, Ana Kata linic 2, Csaba Berec zki3 1 De part ment of Chem is try and En vi ron men tal Sci ences, Uni ver sity of West Hun gary, Szom bathely, Hun gary, e-mail: [email protected] 2 Vrana Lake Nature Park Public Insti tu tion Vrana Lake Nature Park, 23210 Biograd na moru, Croatia 3 Depart ment of Hy drobi ol ogy and Ecology, Uni ver sity of Pécs, Pécs, Hungary

Ab stract Cladocera commu ni ties in sur face sed i ments of seven lakes were sam pled from the Med i ter ra nean to north Hun gary. 2+ 2+ + + – 2– – 2– Con duc tiv ity, pH, pri mary ions (Ca , Mg , Na , K , Cl , SO4 , HCO3 , CO3 ) and macrophyte cover age were mea - sured as con trib uted en vi ron men tal pa ram e ters for the dis tri bu tion of cladoceran com mu ni ties across the lakes. Thirty- two cladoceran species were found in the seven lakes. The recorded species have wide toler ance spectra, and are able to col o nize very dif fer ent kind of hab i tats. The most common and abun dant spe cies were Chydorus sphaericus, Alona rectangula and Bosmina longirostris. Lake area, lat i tude, macrophyte cov er age, pH, con duc tiv ity and hard ness were found to be the most de ter minant en vi ron mental vari ables in the distri bu tion of cladoceran spe cies. This study re - vealed that al though the lakes show a clear sep a ra tion in en vi ron men tal pa ram e ters the com po si tion and dis tri bu tion of Cladoceran com mu ni ties dif fer only slightly across the in ves ti gated geo graph ical gra di ent.

Key words: Subfossil Cladocera, clim ate change, train ing set

INTRO DUC TION in crease is ex pected in the summ er, whilst the smallest in spring. In case of the summ er daily mean tem per ature the ex - Cladocerans are key species in aquatic food-webs, while pected increa se is 4.5–5.1°C (A2) and 3.7–4.2°C (B2). For being nutri ent resource s to other organ ism s and be ing con- spring, the expect ed tem pera ture increa se in Hungary is sum ers of other organ ism s (Eggermont, Martens 2011). Due 2.8–3.3°C (A2) and 2.3–2.7°C (B2). These predic ti ons sug- to this centra l posi ti on in food-webs and to their high repre - gest that an in creas ing Med iter ra nean ef fect on the Hun gar - senta ti on betwee n benthi c and pe lagic taxa, their com muni - ian cli mate is highly proba ble. ties re spond rapidl y to changes in pre dati on pressure and Due to cli ma tic dif fer ences, the sum mer tem per a tures in avail abil ity of nu tri ent re sources (Jeppesen et al. 2011). the Med i ter ra nean lakes ex hibit higher sum mer val ues than Follow ing the pio neer works of Frey (1955, 1958, those in Hungary . Thus, we assum ed that the dif ference s 1959), num erous paleoenvironmental surveys are based on among cladoceran comm u ni ties can be ad dressed to clim ate. Cladocera. Their re mains are well pre served in the sed im ent In this study we com pared cladoceran com muni ti es across a with a bias to the strongly chitinized spe cies (i.e. bosminids cli ma tic gra di ent from the Med i ter ra nean to the Carpathian and chydorids) (Korhola, Rautio 2001; Kattel et al. 2006). Basin. We selec ted lakes from the South (Croatia and Bosnia Thus, these rem ains can be used to recon struc t form er clado- and Herzegovina) to the North (Aggtelek Nati onal Park in ceran com muni ti es espe cia lly those of chydorids. The com - Northern Hungary ) cover ing the broadest spec trum of het er- munit y re sponses of Cladocerans to changes in the physi cal o ge ne ity in wa ter chem is try and hab i tats. This col lec tion of en vi ron ment are gen er ally expressed as changes in spe cies lakes also provides the fundaments for building the “Clado- di ver sity mea sure ments (Hofmann 1987). More over, sev eral cera Train ing-Set” for the Carpathian Ba sin. stud ies have doc u mented the gen eral im por tance of tem per a- ture and other cli mate fac tors to Cladocera comm u nity (Kor- hola, Rautio 2001; Bjerring 2007, Korponai et al. 2011). MATE RIAL AND METHODS Fac ing a global clim ate change, ex treme warm ing is ex - Sur vey area pected with increa sed dry peri ods in the Carpathian ba sin (Gálos et al. 2007). Two scenar ios were construc ted for the The surveys of the seven lakes and ponds (Fig. 1) were pre dic tions of the pos sible ef fect of the clim ate change. Sce - conducte d betwee n April and August, 2011. Two small lakes nario A2 predicted a greater tem per ature in crease in the were se lected in North ern Hun gary. Lake Aggtelek is rel a - Carpathian basin than scenario B2. The larg est tem per ature tively small (1.13 ha) and shal low (aver age depth is 1 m) 46 C. KÖVÉR et al.

in the southeas tern part of the lake, an 800 m long ar ti ficia l chan nel con nects it to the sea (Katalinic et al. 2008). Lake Svitavsko is in Bosnia and Herzegovina, a large ex - panse of moorland, locat ed in the Hutovo Blato Nati onal Park. This lake had been a swamp unti l 1979, but followed by the construc tion of a hy droele ctri c power stati on the swamp was flooded and expanded to a 1,300 ha lake. This is a shallow lake with dense subm erged macrophyte vege ta ti on con- nected to the River Neretva, Hutovo Blato and other lakes through the Krupa River.

En vi ron men tal and chem i cal vari ables Measure ments were taken from a boat at five sampling points at each lake. Phys i cal pa ram e ters such like con duc tiv - ity, tem pera ture and pH were measured in the field using a WQC-24 Multiparameter Wa ter Qual ity Me ter. Macrophyte cover (emerse and sub merse) was es tim ated dur ing walks around the lake by screening the lake bottom in transects with wa ter glass. Water depth and trans par ency were measured using a Secchi disk. Concen tra tion of Na+ and K+ were measured in the lab using a flame spectrophotometer (Flapho 41 , – Zeiss Inc.). SO4 was de ter mined by UV/VIS spectrophoto- 2+ 2+ – 2– meter (Specol, Zeiss Inc.), major ions (Ca , Mg , Cl , CO3 – and HCO3 ) were measured by titrimetry. Further m ore, chlo - ro phyll-a con tent was de ter mined spec tro pho to met ri cally af- ter an extra cti on with metha nol (Wetzel & Likens, 1991). All mea sur ing were con ducted fol low ing ISO pro to cols. The Fig. 1. Map of the study lakes. mean value char acter istic to each lake was cal cu lated from data recorded at five sam pling points. lake, on the border of karstic and non-karstic bedrocks in the Sur face sed i ment sam pling and cladoceran vil lage of Aggtelek. Due to hum an im pact the lake be came anal y sis eutrophic with dense subm ersed vege ta ti on. Lake Vörös is also a small (1 ha), shallow (av er age depth is 1 m) lake near to Sedi m ent sam ples were taken from a boat using a gravit y Lake Aggtelek. Its wa ter is eutrophic and turbid, due to the corer at five points from each lake. The top two centi metres colloi dal clay fracti on (Samu, Bárány-Kevei 2010). of the core was uti lized for fur ther anal yses. Subsamples Lake Velence is larger but also a shallow lake with an av - (1 cm3) for the Cladoceran anal yses were treated with 10% erage depth of 1.89 m, and it is consid ered as a eutrophic, sa - KOH, 10% HCl, and concen tra ted HF solu ti ons and were line and al ka line lake. Its water is dark be cause of the humic then sieved through a 35-µm mesh (Frey 1986), and di luted substa nces. Two main habi tat types include open water and in 10 cm3 of disti lled water . Slides were prepared from 0.1 ml reed beds. The lake suffers from a strong hum an im pact since of each sam ple, and exam ined under a micro scope (100, 200, its coupli ng with Lake Balaton, as a main target for tourism and 400 mag ni fi ca tions). The com po si tion of the Cladoceran (Ács et al. 1994). com mu nity was es ti mated on the ba sis of de ter mi na tion of at Lake Ferto is a large and also a sa line lake, sit u ated be - least 300 indi vid u als in each subsample (Korhola & Rautio tween Hungary and Austri a in the west part of Hungary . Its 2001). Two to six slides from each sam ple were scanned. In trophic state is mesotrophic. Its water is turbid, be cause even cases where less than 300 indi vid u als were counted, the en - small winds (2 m s–1) can mix the shallow wa ter colum n and tire sample was as sessed. To de ter mine the den sity of Clado- stir up the sedi m ent (Löffler 1979). Two main habi tat s can be cerans only well pre served chitinous re mains were taken into identi fied in the lake, the reedbelt (Hungar ian part) and the con sid er ation (headshields, car a paces, postabdomens, post- open wa ter area (Aus trian part). Samples were taken in the abdom inal claws, and ephippia; fragm ents were counted Hungar ian part of the lake. only if un am big u ous di ag nos tic marks were found). Body Lake Baláta is con sid ered as an endorheic peat bog lake parts found most fre quently in the sam ples were used to esti - far from inhab it ed areas with an aver age depth of 1.6 m. This mate the abundance of each taxa per unit vol ume (densit y: in- lake is eutrophic with dense vege ta ti on (Majer et al. 2002). di vid u als cm–3). Rel a tive abun dance were cal cu lated us ing Lake Vrana is a shal low lake (av er age depth of 2.8 m) this raw dataset. Identi fica ti on was carrie d out using the keys with dense, subm erged macrophytes, locat ed in Croatia. The and descri pti ons of Frey (1950, 1962, 1988, 1991), Goulden wa ter is brack ish in this lake par tially due to the nar row, lime - & Frey (1963), Gulyás & Forró (1999), Sebestyén (1965, stone-do lo mite sed i men tary rock bar rier sep a rat ing it from 1969, 1970, 1971), Szeroczyñska & Sarmaja-Korjonen the sea, that are par tially perm eable to salt wa ter. More over, (2007) and Whiteside et al. (1978). The five sam ples from DIS TRI BU TION OF CLADOCERA COM MU NI TIES 47

Fig. 2. Cluster di a gram of lakes by the en vi ron mental pa rame ter (Eucledian dis tance with Ward methods: supper panel), and by cladoceran species (Bray-Curtis dis simi lar ity with Ward methods: lower panel). each lake were counted sep arately, and then a mean value ter, while the large lakes with less macrophyte cover grouped was cal cu lated for each lake for fur ther anal ysis. in the other cluster (Fig. 2 upper panel). The pH varied be - tween 5.4 and 8.6, the conduc ti vit y distri buted in wide range and it varied be tween 73 µS cm–1 and 3860 µS cm–1 (Ta ble 1). Sta tis ti cal anal y sis Ion com posi ti on suggest ed two main lake groups. One Sta tisti cal anal yses were car ried out on the Cladocera group, includ ing Lake Aggtelek, Lake Vörös and Lake Svita- rel ative abun dance data. The Hill’s N2 num bers were cal cu - vsko, was char acter ized by a dom inance of cal cium-hydro - lated for each sam ple and specie s (Hill 1973; Korponai et al. gen-car bon ate ion, whilst the sec ond group, in cor po rat ing 2011). Specie s having a N2 <2 were exclude d from the anal- Lake Ferto and Lake Velence, could be char acter ized with a ysis , the rem oved spe cies ac counting for less than 20% of all so dium-hy dro gen-car bon ate wa ter. Due to wetland en vi ron - the in di vid u als re corded from the sam ples. The rel a tive ment the wa ter chemis try of Lake Baláta was char acter ized abun dance of each species was cal cu lated and values were by calcium -sulphate ion dom inance . Lake Vrana had so- arcsine square root trans formed. The en vi ron men tal pa ram e- dium-chloride type brackish wa ter (Fig. 3). ters were used as a con cen tra tion value, hence pH was con - Thirty-two cladoceran spe cies were found in the seven verted to H+-ion con cen tra tion, then all con cen tra tions were lakes (Ta ble 2). Record ed spe cies have wide tol er ance spec - stan dard ized. tra, and are able to colo nize very differ ent kinds of habi tat s To char ac ter ize lake groups con strained hi er ar chi cal (Korhola & Rautio 2001). The most com mon and most abun- clus ter anal ysis (Ward’s method) was appli ed on Bray-Curtis dant species were Chydorus sphaericus, Alona rectangula dis sim i lar i ties of cladoceran rel a tive abun dances. The same and Bosmina longirostris. The Cladocera comm u ni ties of method was used for en vi ron men tal pa ram e ters based on Lake Vörös and Lake Aggtelek can be char acter ized by the their eu clid ean dis tances. Sim i lar ity Per cent age (SIM PER) pres ence of Dunhevedia crassa. In Lake Baláta, be sides the anal ysis, with a Bray-Curtis measure, was per formed to as - most abundant specie s menti oned above, Alonella excisa oc- sess which taxa are pri maril y re sponsi ble for the observe d curred in high num ber. Al though Lake Ferto and Lake Ve- differ ence s betwee n the lakes groups. Constra ined redun - lence were char acter ized by the high amount of the most dancy anal ysis (RDA), clus ter and sim per analy ses were car - com mon spe cies, the oc cur rence of Oxyurella tenuicaudis ried out on the transform ed data, using R (R De velop m ent was also rem ark able. The Med iter ra nean lakes had dense Core Team, 2010) with vegan package (Oksanen et al. 2010). sub merged macrophyte cover sup port ing abun dant pop u la- tions of Acroperus harpae and Alona affinis (Ta ble 2). Cladocera data yielded DCA gra dient lengths of 1.1927 RE SULTS AND DIS CUS SION and 0.71347 SD for axes 1 and 2, which favours for the use of Lakes showed a strong differ en ti ati on in size and in the redun dancy anal ysis (constra ined RDA). The set current ly amount of macrophyte-cov ered area, since the lakes with have more envi ron m ental param eter s than lakes, and in the high macrophyte cover or small in size grouped in one clus- RDA envi ron m ental data accounte d for 100% of the vari ance 48 C. KÖVÉR et al.

Fig. 3. Maucha di a gram of the ma jor ions.

Ta ble 1 Lake char ac ter is tics and chem i cal pa ram e ters

L. Aggtelek L. Vörös L. Baláta L. Fertõ L. Velence L. Vrana L. Svitavsko Lat i tude (°) 48.47002 48.47311 46.31494 47.73612 47.21514 43.90956 43.021859 Lon gi tude(°) 20.51118 20.54277 17.20676 16.71889 18.61295 15.55744 17.784334 Area (ha) 1.13 1 174 7500* 2800 3000 1300 Macrophyte cover (%) 100 30 100 70 30 70 100 pH 7.5 7.6 5.4 8.6 8.1 8.3 7.1 Con duc tiv ity (µS/cm) 616 179 73.8 2072 1855 3860 259 Chlo ro phyll-a (mg/m3) 56 19 7 12 21 <1 <1 TP (mg/l) 0.349 0.045 0.297 0.051 0.641 0.013 0.026 TN (mg/l) 2.160 0.610 2.900 2.060 2.073 0.1 0.2 Ca++ (mg/l) 92 36 27 38 36 97 53.5 Mg++ (mg/l) 7 3 17 88 203 83 4 Na+ (mg/l) 23 6 1 459 287 660 7 K+ (mg/l) 77 3.9 2.6 37 44 27 0.4 Cl– (mg/l) 5.1 10 8 244 229 1143 11.5 –– SO4 (mg/l) 62 <25 117 372 529 181 0 – HCO3 (mg/l) 311 112 30 481 786 137 166 – CO3 (mg/l) 0 0 0 88 66 0 0 * – Hungar ian part only DIS TRI BU TION OF CLADOCERA COM MU NI TIES 49

Ta ble 2 Rela tive abun dance of Cladocera spe cies

L. Aggtelek L. Vörös L. Baláta L. Fertõ L.Velence L. Vrana L. Svitavsko Acroperus harpae 0.09 4.81 3.45 0.58 2.64 7.66 Alona affinis 0.09 3.45 1.26 0.002 8.02 8.82 Alona costata 0.35 0.16 Alona guttata 5.24 0.96 5.84 0.92 0.15 3.29 17.46 Alona quadrangularis 0.17 0.53 2.54 2.97 Alona rectangula 34.47 8.65 30.5 15.51 47.28 24.07 18.2 Alona sp. 0.35 Alonella excisa 0.96 0.96 10.08 0.04 0.14 3.61 0.06 Alonella exigua 4.77 0.07 0.07 0.09 Alonella nana 2.12 0.27 0.03 8.72 Bosmina longirostris 0.96 2.65 13.14 12.73 34.26 18.64 Camptocercus rectirostris 1.86 0.36 0.35 Ceriodaphnia ephippium 1.48 0.96 0.53 0.06 0.26 0.09 Chydorus sphaericus 32.55 16.35 25.46 39.71 34.18 12.54 10.52 Daph nia longispina-group 0.96 Daph nia magna 1.13 Daph nia pulex-group 7.07 0.96 0.03 Daph nia sp. 0.17 0.96 0.17 0.04 Diaphanosoma sp. 2.8 0.04 Disparalona rostrata 0.96 1.06 0.17 0.02 0.03 0.48 Dunhevedia crassa 14.83 0.96 Eurycercus lamellatus 0.09 0.32 0.09 0.24 0.96 Graptoleberis testudinaria 2.92 0.09 0.29 0.47 Leptodora sp. 0.06 Leydigia acanthocercoides 6.71 1.34 6.43 0.82 Leydigia leydigi 1.59 2.34 0.42 1.4 0.68 Monospilus dispar 0.1 0.002 0.02 0.38 Oxyurella tenuicaudis 0.26 21.15 0.53 14.37 1.82 Pleuroxus laevis 2.88 1.33 0.05 0.1 Pleuroxus trigonellus 0.87 4.81 0.53 0.57 1.12 0.52 1.95 Pleuroxus truncatus 0.17 31.73 0.27 0.01 Pleuroxus unicatus 0.2 Sida crystallina 0.11 Simocephalus sp. 0.96 0.53 0.26 0.09 0.02 in Cladocera data. The eigenvalue of the first two RDA axes Vrana and Lake Svitavsko) large lakes. Although charac ter - were 0.07354 and 0.04938, account ing for 72% of the cum u - istic of Lake Vrana is simi lar to Hun gar ian large lakes (Lake lative vari ance in the cladoceran data. Lake area, lati tude, Velence and Lake Ferto, Fig. 2 upper panel) its Cladocera macrophyte cover, pH, conduc ti vit y and hardness had the com munit y is closer to Lake Svitavsko (Fig. 2 lower panel, low est multicollinearity ([Vari ance In fla tion Fac tor (VIFs)] Fig. 4). Abundance s of A. rectangula, C. sphaericus, B. < 10). It re vealed that they were the most deter minant en vi - longirostris popu la ti ons were greater in large lakes than in ronm ental vari ables in the dis tri buti on of cladoceran spe cies small ones, thus playing a signif i cant role in the sepa ra ti on of (Table 3, Fig. 4). these groups. Moreover, greater popu la ti on sizes of A. rec- The sep ara tion of small lakes was con firmed by clus ter tangula and C. sphaericus were re corded in Hungar ian large anal ysis. Since these small lakes are sit u ated in the north ern - lakes, whilst B. longirostris and A. guttata were more abun - most area, the lati tude ef fect ob trudes size in the RDA analy - dant in the Cro atian lakes. sis (Fig. 4). The second group consis ted of large lakes (Lake We con ducted a sim i lar ity per cent age (SIM PER) anal y - Ferto, Lake Velence, Lake Vrana and Lake Svitavsko) and sis with Bray-Curtis simi lar ity in di ces to in di cate the taxa re - this group can be divided into further groups such as Hungar - spon sible for the fau nal dif fer ences be tween lakes. Macro- ian (Lake Ferto, Lake Velence) and Med iter ra nean (Lake phyte cover, chloro phyl l-a and conduc ti vit y were se lected as 50 C. KÖVÉR et al.

Fig. 4. Re dun dancy anal y sis (RDA) biplot of zoo plank ton spe cies and en vi ron men tal scores. (Acroperus harpae: Acro_harpa, Alona affinis: Alon_affin, A. guttata: Alon_gutta, A. quadrangularis: Alon_quadr, A. rectangula: Alon_recta, Alonella excisa: Alon_excis, Bosmina longirostris: Bosm_longi, Ceriodaphnia ephippium: Ceri_efipp, Chydorus sphaericus: Chyd_sphae, Disparalona rostrata: Disp_rostr, Eurycercus lamellatus: Eury_lamel, Leydigia acanthocercoides: Leyd_acant, L. leydigi: Leyd_leydi, Oxyurella tenuicaudis: Oxyu_tenui, Pleuroxus trigonelus: Pleu_trigo, Simpocephalus sp.: Simo_sp.).

Ta ble 3 specie s can be found in high num ber (Korponai et al. 2010). Vari ance In fla tion Factor of ex plan a tory en vi ron men tal Although in our lake set the macrophyte cover was high, A. vari ables harpae, Pleuroxus sp. and E. lamellatus occurred in high abundance s in Lake Svitavsko only. The bottom of Lake Macro- Conducti- Area Lati tude pH Hard ness Svitavsko was total ly covered by subm erse pondweed phyte cover vity among reed patches, while the cover age on the bottom of 2.488046 1.572175 1.817284 3.568177 4.209104 3.351000 Lake Vrana was lower (70%). Al though A. quadrangularis is regarded as a mud-living spe cies (Korhola & Rautio 2001, Nykänen et al. 2010), it shows a clear rela ti onships with en vi ron men tal fac tors into SIM PER anal y sis. SIM PER re - macrophytes as, in our sam ples, it was found in lakes with vealed that the abundance of A. rectangula and C. sphaericus high macrophyte cover. We found high abundance s of in creased, while that of B. longirostris and A. guttata de- Oxyurella tenuicaudis in Lake Vörös, which is a small lake, creased with in creas ing macrophyte cover. With the in crease and Lake Ferto. This specie s occurs in eutrophic small ponds of chloro phyl l-a content the abundance of A. rectangula and (Boix et al. 2007, Bjerring et al. 2009, Nykänen et al. 2010, C. sphaericus de creased while that of B. longirostris, A. Kattel 2011). Although these lakes were highly differ ent in guttata and A. affinis in creased. These species were re garded most of envi ron m ental vari ables (Ta ble 1, Fig. 2 upper as indi ca tors of moder ate and high trophic sta tus (Chen et al. panel), the com mon charac ter isti c was the high turbid it y. 2010; Korponai et al. 2010), which is in line with the mea- In contra st with our expec ta ti on the Cladocera com mu - sured high chloro phyl l content in these lakes. Be side lat itude, ni ties of the stud ied lakes were very simi lar, con sist ing of conduc ti vit y also had an effect on the abundance of A. comm on species. These lakes were in hab ited by Cladocera rectangula, C. sphaericus, B. longirostris and Leydigia spe cies with wide tol er ance in di cat ing a nar row eco log i cal acanthocercoides. gradi ent length (eigenvalue of first two DCA axes). Due to Our surveys reveal ed that the com posi ti on and dis tri bu - the high propor ti on of gener a li st specie s in our sam ples along tion of Cladoceran com muni ti es only slightly differ across with the higher sen si tiv ity of multivariate or di na tions to spe - the in ves ti gated geo graph ical gra di ent, even though the lakes cialist specie s the power of discri m ina ti on proces s in our show clear sep a ra tion in en vi ron men tal pa ram e ters. Shal low anal ysis was lim ited. The main ecolog i cal drivers could not lakes usuall y have extende d litto ral zone, thus phytophilous be iden tified and still are to be ana lysed us ing a greater sam- DIS TRI BU TION OF CLADOCERA COM MU NI TIES 51 ple set and sta tis ti cal meth ods more sen si tive to gen er a list lat eral head pores in the ge nus Bosmina (Cladocera). Interna- specie s. For study ing the effect of clim ate change, incor po - tionale Re vue gesamten Hydrobiologie 48, 513–522. rat ing other en vi ron men tal pa ram e ters into the anal y sis and Gulyás P., Forró L. 1999. Az ágascsápú rákok (Cladocera) kisha- the exten sion of the data set with other shallow lakes across tározója. Vízi Természet és Könyezetvédelem 9. KGI, Bu da - pest, 2nd edi tion. [A guide for the iden ti fi ca tion of Cladocera the en tire cli ma tic gra di ent have to be se ri ously con sid ered. oc cur ring in Hun gary. In Hun gar ian.] Hill M.O. 1973. Di ver sity and even ness: A unify ing no ta tion and its Ac knowl edge ments con se quences. Ecol ogy 54, 427–432. Hofmann W. 1987. Cladocera in space and time: Anal y sis of lake We are grate ful to Bosnia and Herzegovina Min istry of En vi - sed i ments. Hydrobiologia 145, 315–321. ron ment and Tour ism for permis sion to carry out work on Lake Jeppesen E., Noges P., Davidson T.A., Haberman J., Noges T., Svitavsko, to Melinda Gombár and Ágnes Moldván for tech ni cal Blank K., Lauridsen T.L., Sondergaard M., Sayer C., Laugaste as sistance in the field. This study was fi nan cially supported by, R., Johansson L.S., Bjerring R., Amsinck S.L. 2011. Zoo - TÁMOP 4.2.2-08/1-2008-0020, TÁMOP 4.2.1/B-09/1/KONV- plank ton as in di ca tors in lakes: a sci en tific-based plea for in - 2010-0006. clud ing zoo plank ton in the eco log i cal qual ity as sess ment of lakes ac cord ing to the Eu ro pean Wa ter Frame work Di rec tive REF ER ENCES (WFD). Hydrobiologia 676, 279–297. Katalinic A., Zwicker G., Brozincevic A., Peros-Pucar D., Rubinic Ács É., Buczkó K., Lakatos G. 1994. Changes in the mosaic – like J. 2008. Re la tion be tween hy dro log i cal char ac ter is tics and water sur faces of the Lake Velence as reflected by reed peri- anthropogenic in flu ence in the con text of lake pro tec tion – phyton stud ies. Studia Botanica Hungarica 25, 5–19. case studies of Plitvice Lakes and Vrana Lake in Dalmatia Bjerring R. 2007. Lake re sponse to global change: nu tri ent and cli - (Croatia) BALWOIS– Ohrid, Re pub lic of Mac e donia – 27, 31 mate effects us ing cladoceran (Crustacea) subfossils as prox- May 2008. ies. PhD the sis. Uni ver sity of Aarhus, Den mark, 131pp. Kattel G.R. 2011. Can we im prove man age ment prac tice of flood- Bjerring R., Becares E., Declerck S., Gross E. M., Hansson L.-A., plain lakes using cladoceran zoo plank ton? River Resear ch and Kairesalo T., Nykänen M., Halkiewicz A., Kornijów R., Ap pli ca tions 8, 1113–1120. Conde-Porcuna J.M., Seferlis M., Noges T., Moss B., Amsinck Kattel, G.R., Battarbee R.W., Mackay A., Birks H.J.B. 2006. Are S.L., Odgaard B.V., Jeppesen E. 2009. Subfossil Cladocera in cladoceran fossils in lake sedi ment samples a bi ased reflec tion re la tion to con tem po rary en vi ron men tal vari ables in 54 Pan- of the com muni ties from which they are de rived? Jour nal of Eu ro pean lakes. Fresh wa ter Bi ol ogy 54, 2401–2417. Paleolimnology 38, 157–181. Boix D., Gascón S., Sala J., Badosa A., Brucet S., López-Flores R., Korhola, A., Rautio M. 2001. Cladocera and other Bran chi o pod Martinoy M., Gifre J., Quintana X. D. 2007. Pat terns of com - crus taceans. In. Smol J.P., Birks H.J.B., Last W.M. (Eds.), posi tion and spe cies rich ness of crusta ceans and aquatic in - Track ing En vi ron men tal Change Us ing Lake Sed i ments. Vol - sects along en vi ron men tal gra di ents in Med i ter ra nean wa ter ume 4: Zoo log i cal In di ca tors. 1–38. Kluwer Ac a demic Pub - bod ies. Hydrobiologia 597, 53–69. lish ers, Dordrecht, The Neth er lands. Chen G., Dal ton C., Tay lor D. 2010. Cladocera as in di ca tors of Korponai J., Braun M., Buczkó K., Gyulai I., Forró L., Nédli J., trophic state in Irish lakes. Jour nal of Paleolimnology 44, Papp I. 2010. Transi tion from shal low lake to a wet land: a 465–481. multi-proxy case study in Zalavári Pond, Lake Balaton, Hun- Eggermont H., Mar tens K. 2011. Cladocera crusta ceans: sen ti nels gary. Hydrobiologia 641, 225–244. of en vi ron men tal change. Hydrobiologia 676, 1–7. Korponai J., Magyari E.K., Buczko K., Iepure S., Namiotko T., Frey D.G. 1950. The tax onomic and phylo gen etic sig nif i cance of Czako D., Kövér C., Braun M. 2011. Cladocera re sponse to the head pores of the Chydoridae (Cladocera). Internationale Late Glacial to Early Holo cene climate change in a South Re vue gesamten Hydrobiologie 44, 27 – 50. Carpathian mountain lake. Hydrobiologia 676, 223–235. Frey D.G. 1955. Laangsee: a his tory of meromixis. Memorie Löf?er H. (ed.) 1979. Neusiedlersee, the Lim nol ogy of a Shal low Dell’Istituto Italiano Di Idrobiologia Suppl. 8, 141–164. Lake in Central Europe / Series: Monographiae Biologicae; v. Frey D.G. 1958. The late-glacial cladoceran fauna of a small lake. 37 Publisher: The Hague; Boston: Dr. W. Junk; Hingham, Archiv für Hydrobiologie 54, 209–275. MA:distri bu tion for the U.S. and Can ada, Kluwer Boston. Frey D.G. 1959. The tax onomic and phylo gen etic sig nif i cance of Majer J., Bordács M.M., Borhidi A. 2002. A Baláta-tó vízmino- the head pores of the Chydoridae (Cladocera). Internationale ségének alapállapot felvételezése. Somogyi Múzeumok Közle- Re vue gesamten Hydrobiologie 44, 27–50. ményei 15, 97–106 [Wa ter qual ity moni tor ing of Lake Ba la ta. Frey D.G. 1962. Cladocera from the Eemian inter gla cial of Den - The ref er ence sta tus.] mark. Jour nal of Pa le on tol ogy 36, 1133–1154. Nykänen M., Malinen T., Vakkilainen K., Liukkonen M., Kairesalo Frey D.G. 1986. Cladocera anal y sis. In: B. E. Berglund (ed.), Hand- T. 2010. Cladoceran com munity re sponses to biomanipulation book of palaeooecology and palaeohydrology. John Wiley & and re-oligotrophication in Lake Vesijärvi, Fin land, as in ferred Sons, Chichester, U.S.A.: 692–667. from re mains in an nu ally lam i nated sed i ment. Fresh wa ter Bi - Frey D.G. 1988. Lit to ral and off shore commu ni ties of di a toms, ol ogy 55, 1164–1181. cladocerans and dipterous lar vae, and their in ter pre ta tion in Oksanen J., Blanchet F.G., Kindt R., Legendre P., O’hara R.B., paleolimnology. Jour nal of Paleolimnology 1, 179–191. Simpson G.L., Solymos P., Stevens M.H.H., Wag ner H. 2010. Frey D.G. 1991. First subfossil re cords of Daph nia headshields and vegan: Com munity Ecol ogy Pack age. R pack age ver sion 1.17- shells (Anomopoda, Daphniidae) about 10 000 years old from 4. http://CRAN.R-pro ject.org/pack age=vegan north ern most Greenland, plus Alona guttata (Chydoridae). R De vel opment Core Team 2010. R: A Language and En vi ron ment Jour nal of Paleolimnology 6, 193–197. for Sta tis ti cal Com put ing. R Foun da tion for Sta tis ti cal Com- Gálos B., Lorenz P., Ja cob D. 2007. Will dry events oc cur more of - put ing, Vi enna, Aus tria. ISBN 3-900051-07-0. URL. http:// ten in Hun gary in the fu ture? En vi ron men tal Re search Let ters, www.R-pro ject.org. DOI:10.1088/1748-9326/2/3/034006 Samu A., Bárány-Kevei I. 2010. Water quality char acter iza tion and Goulden C.E., Frey D.G. 1963. The oc cur rence and sig nif i cance of de ter mi na tion of the en vi ron men tal stress on the karstic lakes 52 C. KÖVÉR et al.

in Aggtelek and Slovak karst. In: Barancokova M., Krajci J., i ment of Lake Balaton II. Annales Instituti Biologici (Tihany) Kollár J., Belcakova I., Landscape ecol ogy – meth ods, ap pli - Hungaricae Academie Scientarium 37, 247–279. ca tions and in ter dis ci plin ary ap proach, 471–487. Bratislava. Sebestyén O. 1971. Kladocera tanulmányok a Balatonon IV. Sebestyén O. 1965. Kladocera tanulmányok a Balatonon III. Tótör- Negyedkori maradványok a Balaton üledékében III – Clado- téneti elotanulmányok I – Cladocera studies in Lake Balaton cera stud ies in Lake Balaton IV. Quater nary re mains in the sed- III. Pre lim i nary stud ies for lake his tory in ves ti ga tions. Annales i ment of Lake Balaton III. Annales Instituti Biologici (Tihany) Instituti Biologici (Tihany) Hungaricae Academie Scientarium Hungaricae Academie Scientarium 38, 227–268. 36, 229–256. Szeroczyñska K., Sarmaja-Korjonen K. 2007. At las of subfossil Sebestyén O. 1969. Kladocera tanulmányok a Balatonon IV. Cladocera from cen tral and north ern Eu rope. Friends of the Negyedkori maradványok a Balaton üledékében I – Cladocera Lower Vistula Soci ety, Œwiecie, Poland. studies in Lake Balaton IV. Qua ter nary re mains in the sed i - Wetzel R.G., Lik ens G.E. 1991. Lim no logi cal Anal y ses. Second ment of Lake Balaton I. Annales Instituti Biologici (Tihany) Edi tion. Springer-Verlag. 391 pp. Hungaricae Academie Scientarium 36, 229–256. White side M.C., Wil liams J.B., White C.P. 1978. Sea sonal abun - Sebestyén O. 1970. Kladocera tanulmányok a Balatonon IV. dance and pat tern of Chydorid, Cladocera in mud and veg e ta - Negyedkori maradványok a Balaton üledékében II – Clado- tive hab i tats. Ecol ogy 59, 1177–1188. cera stud ies in Lake Balaton IV. Quater nary re mains in the sed-